Publications by authors named "Wolfram Weckwerth"

192 Publications

Systems biology for crop improvement.

Plant Genome 2021 May 5:e20098. Epub 2021 May 5.

Center of Excellence in Genomics & Systems Biology, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Hyderabad, 502 324, India.

In recent years, generation of large-scale data from genome, transcriptome, proteome, metabolome, epigenome, and others, has become routine in several plant species. Most of these datasets in different crop species, however, were studied independently and as a result, full insight could not be gained on the molecular basis of complex traits and biological networks. A systems biology approach involving integration of multiple omics data, modeling, and prediction of the cellular functions is required to understand the flow of biological information that underlies complex traits. In this context, systems biology with multiomics data integration is crucial and allows a holistic understanding of the dynamic system with the different levels of biological organization interacting with external environment for a phenotypic expression. Here, we present recent progress made in the area of various omics studies-integrative and systems biology approaches with a special focus on application to crop improvement. We have also discussed the challenges and opportunities in multiomics data integration, modeling, and understanding of the biology of complex traits underpinning yield and stress tolerance in major cereals and legumes.
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http://dx.doi.org/10.1002/tpg2.20098DOI Listing
May 2021

The Quest for System-Theoretical Medicine in the COVID-19 Era.

Front Med (Lausanne) 2021 29;8:640974. Epub 2021 Mar 29.

Molecular Systems Biology (MOSYS), University of Vienna, Vienna, Austria.

Precision medicine and molecular systems medicine (MSM) are highly utilized and successful approaches to improve understanding, diagnosis, and treatment of many diseases from bench-to-bedside. Especially in the COVID-19 pandemic, molecular techniques and biotechnological innovation have proven to be of utmost importance for rapid developments in disease diagnostics and treatment, including DNA and RNA sequencing technology, treatment with drugs and natural products and vaccine development. The COVID-19 crisis, however, has also demonstrated the need for systemic thinking and transdisciplinarity and the limits of MSM: the neglect of the bio-psycho-social systemic nature of humans and their context as the object of individual therapeutic and population-oriented interventions. COVID-19 illustrates how a medical problem requires a transdisciplinary approach in epidemiology, pathology, internal medicine, public health, environmental medicine, and socio-economic modeling. Regarding the need for conceptual integration of these different kinds of knowledge we suggest the application of general system theory (GST). This approach endorses an organism-centered view on health and disease, which according to Ludwig von Bertalanffy who was the founder of GST, we call Organismal Systems Medicine (OSM). We argue that systems science offers wider applications in the field of pathology and can contribute to an integrative systems medicine by (i) integration of evidence across functional and structural differentially scaled subsystems, (ii) conceptualization of complex multilevel systems, and (iii) suggesting mechanisms and non-linear relationships underlying the observed phenomena. We underline these points with a proposal on multi-level systems pathology including neurophysiology, endocrinology, immune system, genetics, and general metabolism. An integration of these areas is necessary to understand excess mortality rates and polypharmacological treatments. In the pandemic era this multi-level systems pathology is most important to assess potential vaccines, their effectiveness, short-, and long-time adverse effects. We further argue that these conceptual frameworks are not only valid in the COVID-19 era but also important to be integrated in a medicinal curriculum.
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http://dx.doi.org/10.3389/fmed.2021.640974DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8039135PMC
March 2021

Heat stress response mechanisms in pollen development.

New Phytol 2021 07 20;231(2):571-585. Epub 2021 May 20.

Laboratory of Pollen Biology, Institute of Experimental Botany of the Czech Academy of Sciences, Rozvojová 263, Prague 6, 165 02, Czech Republic.

Being rooted in place, plants are faced with the challenge of responding to unfavourable local conditions. One such condition, heat stress, contributes massively to crop losses globally. Heatwaves are predicted to increase, and it is of vital importance to generate crops that are tolerant to not only heat stress but also to several other abiotic stresses (e.g. drought stress, salinity stress) to ensure that global food security is protected. A better understanding of the molecular mechanisms that underlie the temperature stress response in pollen will be a significant step towards developing effective breeding strategies for high and stable production in crop plants. While most studies have focused on the vegetative phase of plant growth to understand heat stress tolerance, it is the reproductive phase that requires more attention as it is more sensitive to elevated temperatures. Every phase of reproductive development is affected by environmental challenges, including pollen and ovule development, pollen tube growth, male-female cross-talk, fertilization, and embryo development. In this review we summarize how pollen is affected by heat stress and the molecular mechanisms employed during the stress period, as revealed by classical and -omics experiments.
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http://dx.doi.org/10.1111/nph.17380DOI Listing
July 2021

Magnetic Field Induced Changes in the Shoot and Root Proteome of Barley ( L.).

Front Plant Sci 2021 23;12:622795. Epub 2021 Feb 23.

Molecular Systems Biology Lab, Department of Functional and Evolutionary Ecology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.

The geomagnetic field (GMF) has been present since the beginning of plant evolution. Recently, some researchers have focused their efforts on employing magnetic fields (MFs) higher than GMF to improve the seed germination, growth, and harvest of agriculturally important crop plants, as the use of MFs is an inexpensive and environment-friendly technique. In this study, we have employed different treatments of MF at 7 mT (milliTesla) at different time points of exposure, including 1, 3, and 6 h. The extended exposure was followed by five consecutive days at 6 h per day in barley seeds. The results showed a positive impact of MF on growth characteristics for 5-day-old seedlings, including seed germination rate, root and shoot length, and biomass weight. Furthermore, ~5 days of delay of flowering in pre-treated plants was also observed. We used a shotgun proteomics approach to identify changes in the protein signatures of root and shoot tissues under MF effects. In total, we have identified 2,896 proteins. Thirty-eight proteins in the shoot and 15 proteins in the root showed significant changes under the MF effect. Proteins involved in primary metabolic pathways were increased in contrast to proteins with a metal ion binding function, proteins that contain iron ions in their structure, and proteins involved in electron transfer chain, which were all decreased significantly in the treated tissues. The upregulated proteins' overall biological processes included carbohydrate metabolic process, oxidation-reduction process, and cell redox homeostasis, while down-regulated processes included translation and protein refolding. In general, shoot response was more affected by MF effect than root tissue, leading to the identification of 41 shoot specific proteins. This study provides an initial insight into the proteome regulation response to MF during barley's seedling stage.
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http://dx.doi.org/10.3389/fpls.2021.622795DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7940674PMC
February 2021

Physiological and Proteomic Signatures Reveal Mechanisms of Superior Drought Resilience in Pearl Millet Compared to Wheat.

Front Plant Sci 2020 13;11:600278. Epub 2021 Jan 13.

Molecular Systems Biology Lab (MOSYS), Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, Austria.

Presently, pearl millet and wheat are belonging to highly important cereal crops. Pearl millet, however, is an under-utilized crop, despite its superior resilience to drought and heat stress in contrast to wheat. To investigate this in more detail, we performed comparative physiological screening and large scale proteomics of drought stress responses in drought-tolerant and susceptible genotypes of pearl millet and wheat. These chosen genotypes are widely used in breeding and farming practices. The physiological responses demonstrated large differences in the regulation of root morphology and photosynthetic machinery, revealing a stay-green phenotype in pearl millet. Subsequent tissue-specific proteome analysis of leaves, roots and seeds led to the identification of 12,558 proteins in pearl millet and wheat under well-watered and stress conditions. To allow for this comparative proteome analysis and to provide a platform for future functional proteomics studies we performed a systematic phylogenetic analysis of all orthologues in pearl millet, wheat, foxtail millet, sorghum, barley, brachypodium, rice, maize, Arabidopsis, and soybean. In summary, we define (i) a stay-green proteome signature in the drought-tolerant pearl millet phenotype and (ii) differential senescence proteome signatures in contrasting wheat phenotypes not capable of coping with similar drought stress. These different responses have a significant effect on yield and grain filling processes reflected by the harvest index. Proteome signatures related to root morphology and seed yield demonstrated the unexpected intra- and interspecies-specific biochemical plasticity for stress adaptation for both pearl millet and wheat genotypes. These quantitative reference data provide tissue- and phenotype-specific marker proteins of stress defense mechanisms which are not predictable from the genome sequence itself and have potential value for marker-assisted breeding beyond genome assisted breeding.
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http://dx.doi.org/10.3389/fpls.2020.600278DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7838129PMC
January 2021

The TOR-Auxin Connection Upstream of Root Hair Growth.

Plants (Basel) 2021 Jan 13;10(1). Epub 2021 Jan 13.

Molecular Systems Biology (MOSYS), Department of Functional and Evolutionary Ecology, University of Vienna, 1010 Vienna, Austria.

Plant growth and productivity are orchestrated by a network of signaling cascades involved in balancing responses to perceived environmental changes with resource availability. Vascular plants are divided into the shoot, an aboveground organ where sugar is synthesized, and the underground located root. Continuous growth requires the generation of energy in the form of carbohydrates in the leaves upon photosynthesis and uptake of nutrients and water through root hairs. Root hair outgrowth depends on the overall condition of the plant and its energy level must be high enough to maintain root growth. TARGET OF RAPAMYCIN (TOR)-mediated signaling cascades serve as a hub to evaluate which resources are needed to respond to external stimuli and which are available to maintain proper plant adaptation. Root hair growth further requires appropriate distribution of the phytohormone auxin, which primes root hair cell fate and triggers root hair elongation. Auxin is transported in an active, directed manner by a plasma membrane located carrier. The auxin efflux carrier PIN-FORMED 2 is necessary to transport auxin to root hair cells, followed by subcellular rearrangements involved in root hair outgrowth. This review presents an overview of events upstream and downstream of PIN2 action, which are involved in root hair growth control.
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http://dx.doi.org/10.3390/plants10010150DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7828656PMC
January 2021

In Vitro Evaluation of Pro- and Antioxidant Effects of Flavonoid Tricetin in Comparison to Myricetin.

Molecules 2020 Dec 11;25(24). Epub 2020 Dec 11.

Division of Molecular Systems Biology, Department of Functional and Evolutionary Ecology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria.

Flavonoids are rather common plant phenolic constituents that are known for potent antioxidant effects and can be beneficial for human health. Flavonoids with a pyrogallol moiety are highly efficient reducing agents with possible pro- and antioxidant effects, depending on the reaction milieu. Therefore, the redox properties of myricetin and tricetin were investigated by differential pulse voltammetry and deoxyribose degradation assay. Tricetin proved to be a good antioxidant but only showed negligible pro-oxidant activity in one of the deoxyribose degradation assay variants. Compared to tricetin, myricetin showed pro- and antioxidant effects. The more efficient reducing properties of myricetin are probably caused by the positive mesomeric effect of the enolic 3-hydroxy group on ring C. It is evident that the antioxidant properties of structurally similar flavonoids can be converted to apparent pro-oxidant effects by relatively small structural changes, such as hydroxylation. Since reactive oxygen species (ROS) often serve as secondary messengers in pathological and physiological processes in animal and plant cells, the pro- and antioxidant properties of flavonoids are an important part of controlling mechanisms of tissue signal cascades.
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http://dx.doi.org/10.3390/molecules25245850DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7768484PMC
December 2020

Molecular repertoire of Deinococcus radiodurans after 1 year of exposure outside the International Space Station within the Tanpopo mission.

Microbiome 2020 10 29;8(1):150. Epub 2020 Oct 29.

Space Biochemistry Group, Department of Biophysical Chemistry, University of Vienna, Vienna, Austria.

Background: The extraordinarily resistant bacterium Deinococcus radiodurans withstands harsh environmental conditions present in outer space. Deinococcus radiodurans was exposed for 1 year outside the International Space Station within Tanpopo orbital mission to investigate microbial survival and space travel. In addition, a ground-based simulation experiment with conditions, mirroring those from low Earth orbit, was performed.

Methods: We monitored Deinococcus radiodurans cells during early stage of recovery after low Earth orbit exposure using electron microscopy tools. Furthermore, proteomic, transcriptomic and metabolomic analyses were performed to identify molecular mechanisms responsible for the survival of Deinococcus radiodurans in low Earth orbit.

Results: D. radiodurans cells exposed to low Earth orbit conditions do not exhibit any morphological damage. However, an accumulation of numerous outer-membrane-associated vesicles was observed. On levels of proteins and transcripts, a multi-faceted response was detected to alleviate cell stress. The UvrABC endonuclease excision repair mechanism was triggered to cope with DNA damage. Defense against reactive oxygen species is mirrored by the increased abundance of catalases and is accompanied by the increased abundance of putrescine, which works as reactive oxygen species scavenging molecule. In addition, several proteins and mRNAs, responsible for regulatory and transporting functions showed increased abundances. The decrease in primary metabolites indicates alternations in the energy status, which is needed to repair damaged molecules.

Conclusion: Low Earth orbit induced molecular rearrangements trigger multiple components of metabolic stress response and regulatory networks in exposed microbial cells. Presented results show that the non-sporulating bacterium Deinococcus radiodurans survived long-term low Earth orbit exposure if wavelength below 200 nm are not present, which mirrors the UV spectrum of Mars, where CO effectively provides a shield below 190 nm. These results should be considered in the context of planetary protection concerns and the development of new sterilization techniques for future space missions. Video Abstract.
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http://dx.doi.org/10.1186/s40168-020-00927-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7597052PMC
October 2020

Multiomics approach unravels fertility transition in a pigeonpea line for a two-line hybrid system.

Plant Genome 2020 07 18;13(2):e20028. Epub 2020 Jun 18.

Center of Excellence in Genomics & Systems Biology, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Hyderabad, 502 324, India.

Pigeonpea [Cajanus cajan (L.) Millsp.] is a pulse crop cultivated in the semi-arid regions of Asia and Africa. It is a rich source of protein and capable of alleviating malnutrition, improving soil health and the livelihoods of small-holder farmers. Hybrid breeding has provided remarkable improvements for pigeonpea productivity, but owing to a tedious and costly seed production system, an alternative two-line hybrid technology is being explored. In this regard, an environment-sensitive male sterile line has been characterized as a thermosensitive male sterile line in pigeonpea precisely responding to day temperature. The male sterile and fertile anthers from five developmental stages were studied by integrating transcriptomics, proteomics and metabolomics supported by precise phenotyping and scanning electron microscopic study. Spatio-temporal analysis of anther transcriptome and proteome revealed 17 repressed DEGs/DEPs in sterile anthers that play a critical role in normal cell wall morphogenesis and tapetal cell development. The male fertility to sterility transition was mainly due to a perturbation in auxin homeostasis, leading to impaired cell wall modification and sugar transport. Limited nutrient utilization thus leads to microspore starvation in response to moderately elevated day temperature which could be restored with auxin-treatment in the male sterile line. Our findings outline a molecular mechanism that underpins fertility transition responses thereby providing a process-oriented two-line hybrid breeding framework for pigeonpea.
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http://dx.doi.org/10.1002/tpg2.20028DOI Listing
July 2020

Biological nitrification inhibition in the rhizosphere: determining interactions and impact on microbially mediated processes and potential applications.

FEMS Microbiol Rev 2020 11;44(6):874-908

Department of Agriculture, Food, Environment and Forestry, University of Firenze, P.le delle Cascine 28, Firenze 50144, Italy.

Nitrification is the microbial conversion of reduced forms of nitrogen (N) to nitrate (NO3-), and in fertilized soils it can lead to substantial N losses via NO3- leaching or nitrous oxide (N2O) production. To limit such problems, synthetic nitrification inhibitors have been applied but their performance differs between soils. In recent years, there has been an increasing interest in the occurrence of biological nitrification inhibition (BNI), a natural phenomenon according to which certain plants can inhibit nitrification through the release of active compounds in root exudates. Here, we synthesize the current state of research but also unravel knowledge gaps in the field. The nitrification process is discussed considering recent discoveries in genomics, biochemistry and ecology of nitrifiers. Secondly, we focus on the 'where' and 'how' of BNI. The N transformations and their interconnections as they occur in, and are affected by, the rhizosphere, are also discussed. The NH4+ and NO3- retention pathways alternative to BNI are reviewed as well. We also provide hypotheses on how plant compounds with putative BNI ability can reach their targets inside the cell and inhibit ammonia oxidation. Finally, we discuss a set of techniques that can be successfully applied to solve unresearched questions in BNI studies.
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http://dx.doi.org/10.1093/femsre/fuaa037DOI Listing
November 2020

Genomic footprints of repeated evolution of CAM photosynthesis in a Neotropical species radiation.

Plant Cell Environ 2020 12 25;43(12):2987-3001. Epub 2020 Aug 25.

Department of Botany and Biodiversity Research, Division of Systematic and Evolutionary Botany, Faculty of Life Sciences, University of Vienna, Vienna, Austria.

The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by shifts in several adaptive traits or "key innovations" including the transition from C to CAM photosynthesis associated with xeric (heat/drought) adaptation. We used phylogenomic approaches, complemented by differential gene expression (RNA-seq) and targeted metabolite profiling, to address the mechanisms of C /CAM evolution in the extremely species-rich bromeliad genus, Tillandsia, and related taxa. Evolutionary analyses of whole-genome sequencing and RNA-seq data suggest that evolution of CAM is associated with coincident changes to different pathways mediating xeric adaptation in this group. At the molecular level, C /CAM shifts were accompanied by gene expansion of XAP5 CIRCADIAN TIMEKEEPER homologs, a regulator involved in sugar- and light-dependent regulation of growth and development. Our analyses also support the re-programming of abscisic acid-related gene expression via differential expression of ABF2/ABF3 transcription factor homologs, and adaptive sequence evolution of an ENO2/LOS2 enolase homolog, effectively tying carbohydrate flux to abscisic acid-mediated abiotic stress response. By pinpointing different regulators of overlapping molecular responses, our results suggest plausible mechanistic explanations for the repeated evolution of correlated adaptive traits seen in a textbook example of an adaptive radiation.
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http://dx.doi.org/10.1111/pce.13847DOI Listing
December 2020

Mexicanolide-type limonoids from the twigs and leaves of Cipadessa baccifera.

Phytochemistry 2020 Sep 26;177:112449. Epub 2020 Jun 26.

Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, 666303, PR China. Electronic address:

Twelve previously undescribed mexicanolide-type limonoids, including two pairs of isomers, together with seven known analogues were isolated from the twigs and leaves of Cipadessa baccifera. Their structures were determined by extensive spectroscopic methods and electronic circular dichroism (ECD) calculations. Structural variations mainly occurred at the attachment of C-3 and the carbon residues linked to C-17. 21-deoxo-23-oxofebrifugin A and 3-O-detigloyl-3-O-isobutyryl-21-deoxo-23-oxofebrifugin A are two rare naturally occurring mexicanolide-type limonoids bearing an α,β-unsaturated-γ-lactone motif at C-17. Moreover, cipaferen R is the first degraded tetranortriterpenoid derivative featuring an unique acetyl group at C-17. Some isolated compounds were evaluated for nematicidal, antifungal, cytotoxic (against five human cancer cell lines), and acetylcholinesterase inhibitory activities. No nematicidal and antifungal activities were observed, yet 3-O-detigloyl-3-O-isobutyrylfebrifugin A, febrifugin A, febrifugin, and khaysin T exhibited moderate cytotoxic activity against the tested cells with IC values ranging from 18.56 ± 0.27 to 38.00 ± 0.85 μM, and 3-O-detigloyl-3-O-isobutyrylfebrifugin A, granatumin E, khaysin T, and 2'S-cipadesin A showed moderate inhibitory activities against acetylcholinesterase (AChE) at 50 μM.
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http://dx.doi.org/10.1016/j.phytochem.2020.112449DOI Listing
September 2020

Structural and Functional Heat Stress Responses of Chloroplasts of .

Genes (Basel) 2020 06 12;11(6). Epub 2020 Jun 12.

Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, 60438 Frankfurt am Main, Germany.

Temperature elevations constitute a major threat to plant performance. In recent years, much was learned about the general molecular mode of heat stress reaction of plants. The current research focuses on the integration of the knowledge into more global networks, including the reactions of cellular compartments. For instance, chloroplast function is central for plant growth and survival, and the performance of chloroplasts is tightly linked to the general status of the cell and vice versa. We examined the changes in photosynthesis, chloroplast morphology and proteomic composition posed in chloroplasts after a single or repetitive heat stress treatment over a period of two weeks. We observed that the acclimation is potent in the case of repetitive application of heat stress, while a single stress results in lasting alterations. Moreover, the physiological capacity and its adjustment are dependent on the efficiency of the protein translocation process as judged from the analysis of mutants of the two receptor units of the chloroplast translocon, TOC64, and TOC33. In response to repetitive heat stress, plants without TOC33 accumulate Hsp70 proteins and plants without TOC64 have a higher content of proteins involved in thylakoid structure determination when compared to wild-type plants.
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http://dx.doi.org/10.3390/genes11060650DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7349189PMC
June 2020

Molecular Mechanisms of Microbial Survivability in Outer Space: A Systems Biology Approach.

Front Microbiol 2020 15;11:923. Epub 2020 May 15.

Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria.

Since the dawn of space exploration, the survivability of terrestrial life in outer space conditions has attracted enormous attention. Space technology has enabled the development of advanced space exposure facilities to investigate responses of microbial life to the stress conditions of space during interplanetary transfer. Significant progress has been made toward the understanding of the effects of space environmental factors, e.g., microgravity, vacuum and radiation, on microorganisms exposed to real and simulated space conditions. Of extreme importance is not only knowledge of survival potential of space-exposed microorganisms, but also the determination of mechanisms of survival and adaptation of predominant species to the extreme space environment, i.e., revealing the molecular machinery, which elicit microbial survivability and adaptation. Advanced technologies in -omics research have permitted genome-scale studies of molecular alterations of space-exposed microorganisms. A variety of reports show that microorganisms grown in the space environment exhibited global alterations in metabolic functions and gene expression at the transcriptional and translational levels. Proteomic, metabolomic and especially metabolic modeling approaches as essential instruments of space microbiology, synthetic biology and metabolic engineering are rather underrepresented. Here we summarized the molecular space-induced alterations of exposed microorganisms in terms of understanding the molecular mechanisms of microbial survival and adaptation to drastic outer space environment.
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http://dx.doi.org/10.3389/fmicb.2020.00923DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7242639PMC
May 2020

The Potato Yam Phyllosphere Ectosymbiont sp. Msb3 Is a Potent Growth Promotor in Tomato.

Front Microbiol 2020 21;11:581. Epub 2020 Apr 21.

Molecular Systems Biology (MOSYS), Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, Austria.

The genus includes a variety of species with promising features for sustainable biotechnological solutions in agriculture through increasing crop productivity. Here, we present a novel isolate, a permanent and predominant member of the (yam family, ) phyllosphere, making up to 25% of the microbial community on leaf acumens. The 8.5 Mbp genome of isolate Msb3 encodes an unprecedented combination of features mediating a beneficial plant-associated lifestyle, including biological nitrogen fixation (BNF), plant hormone regulation, detoxification of various xenobiotics, degradation of aromatic compounds and multiple protein secretion systems including both T3SS and T6SS. The isolate exhibits significant growth promotion when applied to agriculturally important plants such as tomato, by increasing the total dry biomass by up to 40%. The open question about the "beneficial" nature of this strain led us to investigate ecological and generic boundaries in . In a refined phylogeny including 279 isolates strain Msb3 clusters within Clade I , which also includes few opportunistic strains that can potentially act as pathogens, as revealed by our ecological meta-data analysis. In fact, we demonstrate that all genera originating from the "plant beneficial and environmental" (PBE) species cluster include opportunists. This indicates that further functional examinations are needed before safe application of these strains in sustainable agricultural settings can be assured.
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http://dx.doi.org/10.3389/fmicb.2020.00581DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7186400PMC
April 2020

Mass Spectrometry Untangles Plant Membrane Protein Signaling Networks.

Trends Plant Sci 2020 09 28;25(9):930-944. Epub 2020 Apr 28.

Department of Functional and Evolutionary Ecology, Molecular Systems Biology (MOSYS), University of Vienna, Vienna, 1090, Austria; Vienna Metabolomics Center (VIME), University of Vienna, Vienna, 1090, Austria. Electronic address:

Plasma membranes (PMs) act as primary cellular checkpoints for sensing signals and controlling solute transport. Membrane proteins communicate with intracellular processes through protein interaction networks. Deciphering these signaling networks provides crucial information for elucidating in vivo cellular regulation. Large-scale proteomics enables system-wide characterization of the membrane proteome, identification of ligand-receptor pairs, and elucidation of signals originating at membranes. In this review we assess recent progress in the development of mass spectrometry (MS)-based proteomic pipelines for determining membrane signaling pathways. We focus in particular on current techniques for the analysis of membrane protein phosphorylation and interaction, and how these proteins may be connected to downstream changes in gene expression, metabolism, and physiology.
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http://dx.doi.org/10.1016/j.tplants.2020.03.013DOI Listing
September 2020

Adjustment of photosynthetic activity to drought and fluctuating light in wheat.

Plant Cell Environ 2020 06 27;43(6):1484-1500. Epub 2020 Mar 27.

Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria.

Drought is a major cause of losses in crop yield. Under field conditions, plants exposed to drought are usually also experiencing rapid changes in light intensity. Accordingly, plants need to acclimate to both, drought and light stress. Two crucial mechanisms in plant acclimation to changes in light conditions comprise thylakoid protein phosphorylation and dissipation of light energy as heat by non-photochemical quenching (NPQ). Here, we analyzed the acclimation efficacy of two different wheat varieties, by applying fluctuating light for analysis of plants, which had been subjected to a slowly developing drought stress as it usually occurs in the field. This novel approach allowed us to distinguish four drought phases, which are critical for grain yield, and to discover acclimatory responses which are independent of photodamage. In short-term, under fluctuating light, the slowdown of NPQ relaxation adjusts the photosynthetic activity to the reduced metabolic capacity. In long-term, the photosynthetic machinery acquires a drought-specific configuration by changing the PSII-LHCII phosphorylation pattern together with protein stoichiometry. Therefore, the fine-tuning of NPQ relaxation and PSII-LHCII phosphorylation pattern represent promising traits for future crop breeding strategies.
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http://dx.doi.org/10.1111/pce.13756DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7384038PMC
June 2020

PANOMICS meets germplasm.

Plant Biotechnol J 2020 07 19;18(7):1507-1525. Epub 2020 May 19.

Center of Excellence in Genomics & Systems Biology, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad, Telangana, India.

Genotyping-by-sequencing has enabled approaches for genomic selection to improve yield, stress resistance and nutritional value. More and more resource studies are emerging providing 1000 and more genotypes and millions of SNPs for one species covering a hitherto inaccessible intraspecific genetic variation. The larger the databases are growing, the better statistical approaches for genomic selection will be available. However, there are clear limitations on the statistical but also on the biological part. Intraspecific genetic variation is able to explain a high proportion of the phenotypes, but a large part of phenotypic plasticity also stems from environmentally driven transcriptional, post-transcriptional, translational, post-translational, epigenetic and metabolic regulation. Moreover, regulation of the same gene can have different phenotypic outputs in different environments. Consequently, to explain and understand environment-dependent phenotypic plasticity based on the available genotype variation we have to integrate the analysis of further molecular levels reflecting the complete information flow from the gene to metabolism to phenotype. Interestingly, metabolomics platforms are already more cost-effective than NGS platforms and are decisive for the prediction of nutritional value or stress resistance. Here, we propose three fundamental pillars for future breeding strategies in the framework of Green Systems Biology: (i) combining genome selection with environment-dependent PANOMICS analysis and deep learning to improve prediction accuracy for marker-dependent trait performance; (ii) PANOMICS resolution at subtissue, cellular and subcellular level provides information about fundamental functions of selected markers; (iii) combining PANOMICS with genome editing and speed breeding tools to accelerate and enhance large-scale functional validation of trait-specific precision breeding.
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http://dx.doi.org/10.1111/pbi.13372DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7292548PMC
July 2020

Inverse Data-Driven Modeling and Multiomics Analysis Reveals Phgdh as a Metabolic Checkpoint of Macrophage Polarization and Proliferation.

Cell Rep 2020 02;30(5):1542-1552.e7

Department of Ecogenomics and Systems Biology, University of Vienna, Vienna 1090, Austria; Vienna Metabolomics Center (VIME), University of Vienna, Vienna 1090, Austria. Electronic address:

Mechanistic or mammalian target of rapamycin complex 1 (mTORC1) is an important regulator of effector functions, proliferation, and cellular metabolism in macrophages. The biochemical processes that are controlled by mTORC1 are still being defined. Here, we demonstrate that integrative multiomics in conjunction with a data-driven inverse modeling approach, termed COVRECON, identifies a biochemical node that influences overall metabolic profiles and reactions of mTORC1-dependent macrophage metabolism. Using a combined approach of metabolomics, proteomics, mRNA expression analysis, and enzymatic activity measurements, we demonstrate that Tsc2, a negative regulator of mTORC1 signaling, critically influences the cellular activity of macrophages by regulating the enzyme phosphoglycerate dehydrogenase (Phgdh) in an mTORC1-dependent manner. More generally, while lipopolysaccharide (LPS)-stimulated macrophages repress Phgdh activity, IL-4-stimulated macrophages increase the activity of the enzyme required for the expression of key anti-inflammatory molecules and macrophage proliferation. Thus, we identify Phgdh as a metabolic checkpoint of M2 macrophages.
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http://dx.doi.org/10.1016/j.celrep.2020.01.011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7003064PMC
February 2020

Molecular response of Deinococcus radiodurans to simulated microgravity explored by proteometabolomic approach.

Sci Rep 2019 12 5;9(1):18462. Epub 2019 Dec 5.

Extremophiles/Space Biochemistry Group, Department of Biophysical Chemistry, University of Vienna, Vienna, Austria.

Regarding future space exploration missions and long-term exposure experiments, a detailed investigation of all factors present in the outer space environment and their effects on organisms of all life kingdoms is advantageous. Influenced by the multiple factors of outer space, the extremophilic bacterium Deinococcus radiodurans has been long-termly exposed outside the International Space Station in frames of the Tanpopo orbital mission. The study presented here aims to elucidate molecular key components in D. radiodurans, which are responsible for recognition and adaptation to simulated microgravity. D. radiodurans cultures were grown for two days on plates in a fast-rotating 2-D clinostat to minimize sedimentation, thus simulating reduced gravity conditions. Subsequently, metabolites and proteins were extracted and measured with mass spectrometry-based techniques. Our results emphasize the importance of certain signal transducer proteins, which showed higher abundances in cells grown under reduced gravity. These proteins activate a cellular signal cascade, which leads to differences in gene expressions. Proteins involved in stress response, repair mechanisms and proteins connected to the extracellular milieu and the cell envelope showed an increased abundance under simulated microgravity. Focusing on the expression of these proteins might present a strategy of cells to adapt to microgravity conditions.
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http://dx.doi.org/10.1038/s41598-019-54742-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6895123PMC
December 2019

Dynamics of Plant Metabolism during Cold Acclimation.

Int J Mol Sci 2019 Oct 30;20(21). Epub 2019 Oct 30.

Plant Evolutionary Cell Biology, Department Biology I, Ludwig-Maximilians-Universität München, 82152 Planegg-Martinsried, Bavaria, Germany.

Plants have evolved strategies to tightly regulate metabolism during acclimation to a changing environment. Low temperature significantly constrains distribution, growth and yield of many temperate plant species. Exposing plants to low but non-freezing temperature induces a multigenic processes termed cold acclimation, which eventually results in an increased freezing tolerance. Cold acclimation comprises reprogramming of the transcriptome, proteome and metabolome and affects communication and signaling between subcellular organelles. Carbohydrates play a central role in this metabolic reprogramming. This review summarizes current knowledge about the role of carbohydrate metabolism in plant cold acclimation with a focus on subcellular metabolic reprogramming, its thermodynamic constraints under low temperature and mathematical modelling of metabolism.
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http://dx.doi.org/10.3390/ijms20215411DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6862541PMC
October 2019

Coordination Complex Formation and Redox Properties of Kynurenic and Xanthurenic Acid Can Affect Brain Tissue Homeodynamics.

Antioxidants (Basel) 2019 Oct 11;8(10). Epub 2019 Oct 11.

Division of Molecular Systems Biology, Department of Ecogenomics and Systems Biology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria.

Reactive oxygen species (ROS) are known for their participation in various physiological and pathological processes in organisms, including ageing or degeneration. Kynurenine pathway metabolites, such as kynurenic (KYNA) or xanthurenic (XA) acid, can affect neurodegenerative diseases due to their ROS scavenging and Fe ion coordination complex formation but insights are still incomplete. Therefore, we investigated the formation and antioxidant capabilities of KYNA- and XA-Fe complexes by nano-electrospray-mass spectrometry, differential pulse voltammetry, deoxyribose degradation and Fe autoxidation assays. XA formed coordination complexes with Fe or Fe ions and was an effective antioxidant. By contrast, only Fe-KYNA complexes could be detected. Moreover, KYNA showed no antioxidant effects in the FeCl/ascorbic acid deoxyribose degradation assay variant and only negligible activities in the Fe autoxidation assay. Coordination complexes of Fe ions with KYNA probably stabilize KYNA in its keto tautomer form. Nevertheless, both KYNA and XA exhibited sufficient antioxidant activities in some of the employed assay variants. The results provide evidence that both have the potential to alleviate neurodegenerative diseases by helping to maintain tissue redox homeodynamics.
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http://dx.doi.org/10.3390/antiox8100476DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6826357PMC
October 2019

The High Light Response in Arabidopsis Requires the Calcium Sensor Protein CAS, a Target of STN7- and STN8-Mediated Phosphorylation.

Front Plant Sci 2019 30;10:974. Epub 2019 Jul 30.

Plant Cell Biology, Institut für Zelluläre und Molekulare Botanik, University of Bonn, Bonn, Germany.

Reversible phosphorylation of thylakoid proteins contributes to photoacclimation responses in photosynthetic organisms, enabling the fine-tuning of light harvesting under changing light conditions and promoting the onset of photoprotective processes. However, the precise functional role of many of the described phosphorylation events on thylakoid proteins remains elusive. The calcium sensor receptor protein (CAS) has previously been indicated as one of the targets of the state transition kinase 8 (STN8). Here we show that in , CAS is also phosphorylated by the state transition kinase 7 (STN7), as well as by another, so-far unknown, Ca-dependent kinase. Phosphoproteomics analysis and phosphorylation assays on CAS variants identified the phylogenetically conserved residues Thr-376, Ser-378, and Thr-380 as the major phosphorylation sites of the STN kinases. Spectroscopic analyses of chlorophyll fluorescence emission at 77K further showed that, while the mutant is not affected in state transition, it displays a persistent strong excitation of PSI under high light exposure, similar to the phenotype previously observed in other mutants defective in photoacclimation mechanisms. Together with the observation of a strong concomitant phosphorylation of light harvesting complex II (LHCII) and photosynthetic core proteins under high irradiance in the mutant this suggests a role for CAS in the STN7/STN8/TAP38 network of phosphorylation-mediated photoacclimation processes in Arabidopsis.
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http://dx.doi.org/10.3389/fpls.2019.00974DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6682602PMC
July 2019

Subcellular dynamics of proteins and metabolites under abiotic stress reveal deferred response of the Arabidopsis thaliana hexokinase-1 mutant gin2-1 to high light.

Plant J 2019 11 25;100(3):456-472. Epub 2019 Sep 25.

Department of Plant Biotechnology, Institute of Biomaterials and Biomolecular Systems, University of Stuttgart, Pfaffenwaldring 57, 70569, Stuttgart, Germany.

Stress responses in plants imply spatio-temporal changes in enzymes and metabolites, including subcellular compartment-specific re-allocation processes triggered by sudden changes in environmental parameters. To investigate interactions of primary metabolism with abiotic stress, the gin2-1 mutant, defective in the sugar sensor hexokinase 1 (HXK1) was compared with its wildtype Landsberg erecta (Ler) based on time resolved, compartment-specific metabolome and proteome data obtained over a full diurnal cycle. The high light sensitive gin2-1 mutant was substantially delayed in subcellular re-distribution of metabolites upon stress, and this correlated with a massive reduction in proteins belonging to the ATP producing electron transport chain under high light, while fewer changes occurred in the cold. In the wildtype, compounds specifically protecting individual compartments could be identified, e.g., maltose and raffinose in plastids, myo-inositol in mitochondria, but gin2-1 failed to recruit these substances to the respective compartments, or responded only slowly to high irradiance. No such delay was obtained in the cold. At the whole cell level, concentrations of the amino acids, glycine and serine, provided strong evidence for an important role of the photorespiratory pathway during stress exposure, and different subcellular allocation of serine may contribute to the slow growth of the gin2-1 mutant under high irradiance.
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http://dx.doi.org/10.1111/tpj.14491DOI Listing
November 2019

Male Sterility in Maize after Transient Heat Stress during the Tetrad Stage of Pollen Development.

Plant Physiol 2019 10 4;181(2):683-700. Epub 2019 Aug 4.

University of Regensburg, Cell Biology and Plant Biochemistry, 93053 Regensburg, Germany

Shifts in the duration and intensity of ambient temperature impair plant development and reproduction, particularly male gametogenesis. Stress exposure causes meiotic defects or premature spore abortion in male reproductive organs, leading to male sterility. However, little is known about the mechanisms underlying stress and male sterility. To elucidate these mechanisms, we imposed a moderate transient heat stress on maize () plants at the tetrad stage of pollen development. After completion of pollen development at optimal conditions, stress responses were assessed in mature pollen. Transient heat stress resulted in reduced starch content, decreased enzymatic activity, and reduced pollen germination, resulting in sterility. A transcriptomic comparison pointed toward misregulation of starch, lipid, and energy biosynthesis-related genes. Metabolomic studies showed an increase of Suc and its monosaccharide components, as well as a reduction in pyruvate. Lipidomic analysis showed increased levels of unsaturated fatty acids and decreased levels of saturated fatty acids. In contrast, the majority of genes involved in developmental processes such as those required for auxin and unfolded protein responses, signaling, and cell wall biosynthesis remained unaltered. It is noteworthy that changes in the regulation of transcriptional and metabolic pathway genes, as well as heat stress proteins, remained altered even though pollen could recover during further development at optimal conditions. In conclusion, our findings demonstrate that a short moderate heat stress during the highly susceptible tetrad stage strongly affects basic metabolic pathways and thus generates germination-defective pollen, ultimately leading to severe yield losses in maize.
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http://dx.doi.org/10.1104/pp.19.00707DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6776839PMC
October 2019

Resolving subcellular plant metabolism.

Plant J 2019 11 25;100(3):438-455. Epub 2019 Sep 25.

Department Biology I, Plant Evolutionary Cell Biology, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Germany.

Plant cells are characterized by a high degree of compartmentalization and a diverse proteome and metabolome. Only a very limited number of studies has addressed combined subcellular proteomics and metabolomics which strongly limits biochemical and physiological interpretation of large-scale 'omics data. Our study presents a methodological combination of nonaqueous fractionation, shotgun proteomics, enzyme activities and metabolomics to reveal subcellular diurnal dynamics of plant metabolism. Subcellular marker protein sets were identified and enzymatically validated to resolve metabolism in a four-compartment model comprising chloroplasts, cytosol, vacuole and mitochondria. These marker sets are now available for future studies that aim to monitor subcellular metabolome and proteome dynamics. Comparing subcellular dynamics in wild type plants and HXK1-deficient gin2-1 mutants revealed a strong impact of HXK1 activity on metabolome dynamics in multiple compartments. Glucose accumulation in the cytosol of gin2-1 was accompanied by diminished vacuolar glucose levels. Subcellular dynamics of pyruvate, succinate and fumarate amounts were significantly affected in gin2-1 and coincided with differential mitochondrial proteome dynamics. Lowered mitochondrial glycine and serine amounts in gin2-1 together with reduced abundance of photorespiratory proteins indicated an effect of the gin2-1 mutation on photorespiratory capacity. Our findings highlight the necessity to resolve plant metabolism to a subcellular level to provide a causal relationship between metabolites, proteins and metabolic pathway regulation.
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http://dx.doi.org/10.1111/tpj.14472DOI Listing
November 2019

Proteomic and Metabolomic Profiling of Recovering After Exposure to Simulated Low Earth Orbit Vacuum Conditions.

Front Microbiol 2019 29;10:909. Epub 2019 Apr 29.

Department of Biophysical Chemistry, University of Vienna, Vienna, Austria.

The polyextremophile, gram-positive bacterium can withstand harsh conditions of real and simulated outer space environment, e.g., UV and ionizing radiation. A long-term space exposure of has been performed in Low Earth Orbit (LEO) in frames of the Tanpopo orbital mission aiming to investigate the possibility of interplanetary life transfer. Space vacuum (10 -10 Pa) is a harmful factor, which induces dehydration and affects microbial integrity, severely damaging cellular components: lipids, carbohydrates, proteins, and nucleic acids. However, the molecular strategies by which microorganisms protect their integrity on molecular and cellular levels against vacuum damage are not yet understood. In a simulation experiment, we exposed dried cells to vacuum (10 -10 Pa), which resembles vacuum pressure present outside the International Space Station in LEO. After 90 days of high vacuum exposure, survival of cells was 2.5-fold lower compared to control cells. To trigger molecular repair mechanisms, vacuum exposed cells of were recovered in complex medium for 3 and 6 h. The combined approach of analyzing primary metabolites and proteins revealed important molecular activities during early recovery after vacuum exposure. In total, 1939 proteins covering 63% of annotated protein sequences were detected. Proteases, tRNA ligases, reactive oxygen species (ROS) scavenging proteins, nucleic acid repair proteins, TCA cycle proteins, and -layer proteins are highly abundant after vacuum exposure. The overall abundance of amino acids and TCA cycle intermediates is reduced during the recovery phase of as they are needed as carbon source. Furthermore, vacuum exposure induces an upregulation of Type III histidine kinases, which trigger the expression of -layer related proteins. Along with the highly abundant transcriptional regulator of FNR/CRP family, specific histidine kinases might be involved in the regulation of vacuum stress response. After repair processes are finished, switches off the connected repair machinery and focuses on proliferation. Combined comparative analysis of alterations in the proteome and metabolome helps to identify molecular key players in the stress response of , thus elucidating the mechanisms behind its extraordinary regenerative abilities and enabling this microorganism to withstand vacuum stress.
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http://dx.doi.org/10.3389/fmicb.2019.00909DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6501615PMC
April 2019

Combination of Hypoglycemia and Metformin Impairs Tumor Metabolic Plasticity and Growth by Modulating the PP2A-GSK3β-MCL-1 Axis.

Cancer Cell 2019 05 25;35(5):798-815.e5. Epub 2019 Apr 25.

Department of Experimental Oncology, IEO, European Institute of Oncology IRCCS, via Adamello 16, 20139 Milan, Italy; Department of Biosciences, University of Milan, 20100 Milan, Italy. Electronic address:

Tumor cells may adapt to metabolic challenges by alternating between glycolysis and oxidative phosphorylation (OXPHOS). To target this metabolic plasticity, we combined intermittent fasting, a clinically feasible approach to reduce glucose availability, with the OXPHOS inhibitor metformin. In mice exposed to 24-h feeding/fasting cycles, metformin impaired tumor growth only when administered during fasting-induced hypoglycemia. Synergistic anti-neoplastic effects of the metformin/hypoglycemia combination were mediated by glycogen synthase kinase 3β (GSK3β) activation downstream of PP2A, leading to a decline in the pro-survival protein MCL-1, and cell death. Mechanistically, specific activation of the PP2A-GSK3β axis was the sum of metformin-induced inhibition of CIP2A, a PP2A suppressor, and of upregulation of the PP2A regulatory subunit B56δ by low glucose, leading to an active PP2A-B56δ complex with high affinity toward GSK3β.
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http://dx.doi.org/10.1016/j.ccell.2019.03.007DOI Listing
May 2019

Molecular Mechanisms of Tungsten Toxicity Differ for Depending on Nitrogen Regime.

Front Plant Sci 2019 2;10:367. Epub 2019 Apr 2.

Department of Forest and Soil Sciences, Institute of Soil Research, University of Natural Resources and Life Sciences Vienna, Tulln, Austria.

Tungsten (W) finds increasing application in military, aviation and household appliance industry, opening new paths into the environment. Since W shares certain chemical properties with the essential plant micronutrient molybdenum (Mo), it is proposed to inhibit enzymatic activity of molybdoenzymes [e.g., nitrate reductase (NR)] by replacing the Mo-ion bound to the co-factor. Recent studies suggest that W, much like other heavy metals, also exerts toxicity on its own. To create a comprehensive picture of tungsten stress, this study investigated the effects of W on growth and metabolism of soybean (), depending on plant nitrogen regime [nitrate fed (N fed) vs. symbiotic N fixation (N fix)] by combining plant physiological data (biomass production, starch and nutrient content, N fixation, nitrate reductase activity) with root and nodule proteome data. Irrespective of N regime, NR activity and total N decreased with increasing W concentrations. Nodulation and therefore also N fixation strongly declined at high W concentrations, particularly in N fix plants. However, N fixation rate (g N fixed g nodule dwt) remained unaffected by increasing W concentrations. Proteomic analysis revealed a strong decline in leghemoglobin and nitrogenase precursor levels (NifD), as well as an increase in abundance of proteins involved in secondary metabolism in N fix nodules. Taken together this indicates that, in contrast to the reported direct inhibition of NR, N fixation appears to be indirectly inhibited by a decrease in nitrogenase synthesis due to W induced changes in nodule oxygen levels of N fix plants. Besides N metabolism, plants exhibited a strong reduction of shoot (both N regimes) and root (N fed only) biomass, an imbalance in nutrient levels and a failure of carbon metabolic pathways accompanied by an accumulation of starch at high tungsten concentrations, independent of N-regime. Proteomic data (available via ProteomeXchange with identifier PXD010877) demonstrated that the response to high W concentrations was independent of nodule functionality and dominated by several peroxidases and other general stress related proteins. Based on an evaluation of several W responsive proteotypic peptides, we identified a set of protein markers of W stress and possible targets for improved stress tolerance.
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http://dx.doi.org/10.3389/fpls.2019.00367DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6454624PMC
April 2019

Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes.

Ecol Lett 2019 Jan 22;22(1):159-169. Epub 2018 Nov 22.

School of Earth and Environmental Sciences, The University of Manchester, Manchester, M13 9PL, UK.

Climate warming affects plant physiology through genetic adaptation and phenotypic plasticity, but little is known about how these mechanisms influence ecosystem processes. We used three elevation gradients and a reciprocal transplant experiment to show that temperature causes genetic change in the sedge Eriophorum vaginatum. We demonstrate that plants originating from warmer climate produce fewer secondary compounds, grow faster and accelerate carbon dioxide (CO ) release to the atmosphere. However, warmer climate also caused plasticity in E. vaginatum, inhibiting nitrogen metabolism, photosynthesis and growth and slowing CO release into the atmosphere. Genetic differentiation and plasticity in E. vaginatum thus had opposing effects on CO fluxes, suggesting that warming over many generations may buffer, or reverse, the short-term influence of this species over carbon cycle processes. Our findings demonstrate the capacity for plant evolution to impact ecosystem processes, and reveal a further mechanism through which plants will shape ecosystem responses to climate change.
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http://dx.doi.org/10.1111/ele.13178DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6334510PMC
January 2019